Degradation of the Plant Defense Signal Salicylic Acid Protects Ralstonia solanacearum from Toxicity and Enhances Virulence on Tobacco.

Tiffany M Lowe-Power,Caitilyn Allen,Philippe Prior,Florent Ailloud,Brianna Fochs,Jonathan M Jacobs,Steven E Lindow

doi:10.1128/mbio.00656-16

Abstract

ABSTRACTPlants use the signaling molecule salicylic acid (SA) to trigger defenses against diverse pathogens, including the bacterial wilt pathogen Ralstonia solanacearum. SA can also inhibit microbial growth. Most sequenced strains of the heterogeneous R. solanacearum species complex can degrade SA via gentisic acid to pyruvate and fumarate. R. solanacearum strain GMI1000 expresses this SA degradation pathway during tomato pathogenesis. Transcriptional analysis revealed that subinhibitory SA levels induced expression of the SA degradation pathway, toxin efflux pumps, and some general stress responses. Interestingly, SA treatment repressed expression of virulence factors, including the type III secretion system, suggesting that this pathogen may suppress virulence functions when stressed. A GMI1000 mutant lacking SA degradation activity was much more susceptible to SA toxicity but retained the wild-type colonization ability and virulence on tomato. This may be because SA is less important than gentisic acid in tomato defense signaling. However, another host, tobacco, responds strongly to SA. To test the hypothesis that SA degradation contributes to virulence on tobacco, we measured the effect of adding this pathway to the tobacco-pathogenic R. solanacearum strain K60, which lacks SA degradation genes. Ectopic addition of the GMI1000 SA degradation locus, including adjacent genes encoding two porins and a LysR-type transcriptional regulator, significantly increased the virulence of strain K60 on tobacco. Together, these results suggest that R. solanacearum degrades plant SA to protect itself from inhibitory levels of this compound and also to enhance its virulence on plant hosts like tobacco that use SA as a defense signal molecule.

Highlights

Salicylic acid (SA) is a key signaling molecule for plant defense against certain pathogens [1, 2]
Since salicylic acid (SA) levels increase in a broad diversity of plants responding to microbial infection [23], and we previously showed that expression of genes in the SA defense pathway increases in tomato and tobacco plants infected with R. solanacearum
We show that the SA degradation pathway is conserved in most R. solanacearum isolates with sequenced genomes

Summary

Introduction

Salicylic acid (SA) is a key signaling molecule for plant defense against certain pathogens [1, 2]. Host recognition of effectors may activate defense signaling pathways, including the SA pathway, leading to effector-triggered immunity [11]. The result of these signals is either quantitative resistance that slows pathogen growth or rapid programmed cell death, known as the hypersensitive response (HR). The genome of strain GMI1000 contains the seven-gene nagAaGHAbIKL locus predicted to encode the degradation of SA to Krebs cycle intermediates (Fig. 1A) [24,25,26,27] These genes are expressed by R. solanacearum cells growing in tomato xylem [28, 29]. We demonstrate that ectopic expression of the SA degradation genes in R. solanacearum strain K60 increases its virulence on tobacco plants

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Conclusion